Ann Microbiol (2014) 64:921–934 DOI 10.1007/s13213-014-0911-2 REVIEW ARTICLE The prevalence of antibiotic resistance genes among Aeromonas species in aquatic environments Marta Piotrowska & Magdalena Popowska Received: 10 January 2014 /Accepted: 5 May 2014 /Published online: 23 May 2014 # Springer-Verlag Berlin Heidelberg and the University of Milan 2014 Abstract The global rise in antimicrobial resistance (AMR) Keywords Aeromonas . Antibiotic resistance genes . Natural among bacteria causing infectious diseases is well documented, water . Aquacultures . Urban drinking water . Wastewater and the associated risks for human health are well known. There treatment plant is much less research on AMR with regard to environmental strains, both opportunistic and pathogenic ones. The genus Aeromonas is widely distributed in the environment and causes Introduction many variable diseases in fish and humans. Infections in humans are predominantly caused by Aeromonas veronii, A. hydrophila Species belonging to the genus Aeromonas are widely distrib- and A. caviae (A. punctata) in a form of bacteremia, gastroen- uted in the environment. They are able to inhabit natural soil, teritis or even septicaemia in immunocompetent and immuno- food and animals, but they most commonly occur in all kinds compromised individuals. Different groups of antibiotics are of aquatic environments (Janda and Abott 2010). Aeromonas used in the treatment, but studies indicate that fluoroquinolones spp. have been isolated from wastewater (Figueira et al. 2011), and cefotaxime are the most efficient. A disturbing consequence natural water such as rivers, lakes and estuaries (Henriques of antibiotic overuse is an increasing number of detection of et al. 2006; Picão et al. 2008), aquacultures (Schmidt et al. various antibiotic resistance genes (ARG) within this genus. The 2001; Sørum 2006) and urban drinking water (Carvalho et al. water environment is one of the major modes of transmission of 2012). The genus Aeromonas has a complex taxonomy at the resistant bacteria from animals to humans, and, thus, the dis- species level, but it belongs to the family Aeromondaceae, semination of antibiotic resistance genes, particularly those which is part of the class of Gamma-proteobacteria. The located in mobile genetic elements (MGE) occurs in such as species classification changes dynamically with the emer- plasmids and transposons. This review summarizes recently gence of new genetic analyses, but thus far 28 species have published information on the type, distribution, and transmission been validated or proposed (http://www.bacterio.net). of ARG by MGE, widespread in Aeromonas strains living in Aeromonas species belong to one of the two major groups: various aquatic environments, including wastewater, natural psychrophilic or mesophilic bacteria. The former represents water, aquaculture and urban drinking water. The data available nonmotile bacteria with optimal growth temperature balanced indicate that the opportunistic pathogens like Aeromonas spp. between 22 - 25 °C that cause many variable diseases in fish, might serve as important vectors of ARG for clinically relevant e.g., furunculosis, septicaemia, ulcerative or hemorrhagic dis- pathogens present in such bodies of water . eases (Beaz-Hidalgo and Figueras 2013; Dallaire-Dufresne et al. 2013). In contrast, mesophilic species are motile, their : optimal growth temperature is between 35 - 37 °C, and being M. Piotrowska M. Popowska opportunistic pathogens of humans, they are potentially dan- Department of Applied Microbiology, Institute of Microbiology, Faculty of Biology, University of Warsaw, Miecznikowa 1, gerous. Infections are mostly induced by A. veronii, A. 02-096 Warsaw, Poland hydrophila and A. caviae (A. punctata) and result in bacter- emia, gastroenteritis or even septicaemia in immunocompe- * M. Piotrowska ( ) tent and immunocompromised individuals (Lai et al. 2007; Institute of Microbiology, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland Parker and Shaw 2010). The number of infectious cases e-mail: [email protected] increases in the warmer months and the most common 922 Ann Microbiol (2014) 64:921–934 manifestations are diarrhea and skin infections after contact conditions for the proliferation of bacteria (richness of nutri- with contaminated water. Treatment of these infections varies ents, aeration, optimal temperature). Particularly favorable and depends on the part of the world, but studies indicate that conditions exist in the activated sludge, which is characterized fluoroquinolones and cefotaxime are the most successful ther- by a high density and variety of microorganisms. Moreover, apies (Parker and Shaw 2010). Aeromonas infections are not WWTP receive large amounts of antibiotics with sewage an important public health problem so epidemiology is not water from hospitals, livestock manure and private house- very well known. However, previous studies carried out in holds, where bacteria are exposed to selection pressure different countries suggested that these infections should not (Bouki et al. 2013). These conditions promote the prolifera- be underestimated (Ghenghesh et al. 2008). Given the fact that tion of antibiotic resistant bacteria (ARB) and increase the Aeromonas spp. are opportunistic pathogens of humans and probability of the horizontal gene transfer (HGT) of ARG the causative agent of fish diseases, it is disturbing that more (Tennstedt et al. 2003). and more different antibiotic resistance genes (ARG) are being The study on sewage samples using high-throughput se- detected within this genus (Zhang et al. 2009a). The main quencing of 16S rRNA gene has detected over ten bacterial targets of Aeromonas are fish, which are exposed to these phyla with the highest contribution being from Proteobacteria, natural pathogens. To study the prevalence and horizontal Actinobactera, Chloroflexi, Firmicutes, Bacteriodetes and transfer of resistance genes within this genus, it is important Nitrospirae (Ye et al. 2012) as well as a large number of to examine the aquatic environment as a whole, including fish Aeromonas spp. (Moura et al. 2007; Figueira et al. 2011; and sediments. Igbinosa and Okoh 2012; Moura et al. 2012;Igbinosaand ARG are ubiquitous both in clinical pathogens and envi- Okoh 2013). Treatment processes reduce bacterial count in the ronmental bacterial species. This is in part due to the wide sewage, including the ARB (Guardabassi et al. 2002). How- usage of antibiotics in clinical practice, veterinary medicine ever, even in effluent water, ARG can be taken up by trans- and agriculture (Cantas et al. 2013), resulting in the release of formation and ARB are still detected (Zhang et al. 2009a). large amounts of these pollutants to the environment. Antibi- In the literature there is little information about ARG in otics, in addition to being chemical pollutants, exert a selective Aeromonas spp. present in WWTP. A variety of different pressure retaining and spreading the ARG among microbiota, species that has been detected so far include which poses a risk to human health (Kemper 2008). Addition- A. allosaccharophila, A. aquariorum, A. hydrophila, A. me- ally, it has been demonstrated that heavy metals can co-select dia, A. veronii, A. caviae, A. sanarellii and A. taiwanesis, the spread of ARG in the environment (Seiler and Berendonk (Figueira et al. 2011) (Table 1). The ARG recently found in 2012). Consequently, natural environments, especially water Aeromonas strains from wastewater encoded resistance to four bodies, constitute important reservoirs of ARG that may pro- major groups of antibiotics, i.e., the quinolones, aminoglyco- mote the spread of resistance to different groups of antibiotics sides, β-lactams and tetracyclines. In contrast to previous across different bacterial species (Lupo et al. 2012). Hence, studies, Figueira et al. (2011) who isolated bacteria from opportunistic pathogens such as Aeromonas spp. might be municipal sewage, argued that the vast majority of quinolone dangerous vectors of ARG for clinically relevant pathogens, resistance was the result of chromosomal mutations. These which also occur in the water (Rhodes et al. 2000;Sørum authors found many mutations in gyrA and parC genes, which 2006). are genetic determinants of quinolone resistance. The majority In this review we strive to present the latest information of these strains was resistant to nalidixic acid and belonged to from the literature on the prevalence of ARG in Aeromonas A. media and A. caviae species. This high frequency of muta- spp. from various water environments endowed with different tions could be the effect of contact with a high concentration anthropogenic impact. The main focus is on the differences of mutagenic substances in wastewater (Miyahara et al. 2011). between natural water, drinking water and more polluted These authors also found two plasmid-mediated quinolone environments such as wastewater and aquacultures. Further, resistance genes: qnrS and accA-cr, but only in A. media our intent is to highlight the problem of the horizontal transfer strains. In addition, this study investigated the occurrence of of these genes, which is related to the presence of integrons the cphA chromosomal gene, which is the most common and mobile genetic elements such as plasmids, transposons or metallo-β-lactamase in Aeromonas spp. (Janda and Abott insertion sequences, and the serious risks for human health 2010). This gene was detected in 18 % of strains